Bioaccumulation Factor of Selected Heavy Metals in Zea mays

Background. Health risks arising from heavy metal pollution have attracted global attention. As a result, many studies on the accumulation of heavy metals in soil-plant systems have performed human health risk assessments. Objectives. We aimed to examine the ability of Zea mays (maize) to accumulate heavy metals and assess the bioaccumulation factor (BAF) by collecting, collating, and analyzing data on heavy metal concentrations in Zea mays. Methods. This study reviewed the accumulation of five selected heavy metals, cadmium (Cd), chromium (Cr), lead (Pb), copper (Cu), and zinc (Zn) in soil and the corresponding BAF of Zea mays grown on those soils using a systematic search of peer-reviewed scientific journals. A total of 27 research works were reviewed after screening 52 articles for subject matter relevancy, including dumpsites, industrially polluted soils, inorganically fertilized soils, mining sites, smelting sites, municipal wastewater irrigated soils, and a battery waste dumpsite. Results. Among the reviewed sites, concentrations of Cd and Cr were highest at a tin mining site, where prolonged mining, mineral processing and other production activities contributed heavy metal pollution in the soil. The soil at a battery waste dumpsite exhibited the highest Pb concentration, while the soil at a Zn smelting site presented the highest concentration of Zn. The highest soil Cu concentration was found in an area where sewage irrigation had been carried out over a long period. The BAF of the five heavy metals in Zea mays increased with the metal concentrations in the soil. The BAF of Cd, Cr, Pb, Cu, and Zn in Zea mays from the study areas fall within the ranges of 0–0.95, 0–1.89, 0–1.20, 0.011–0.99, and 0.03–0.99, respectively. Cadmium and Zn had the highest bioconcentration factors values in maize plants, likely due to their higher mobility rate compared to the other heavy metals. Conclusions. The study concluded that Zea mays is capable of accumulating high amounts of heavy metals, although accumulation of these heavy metals is influenced by multiple factors including soil texture, cation exchange capacity, root exudation and especially soil pH and chemical forms of the heavy metals. Zea mays should not be planted on metal-contaminated soils because of its potential to act as a hyperaccumulator. Competing Interests. The authors declare no competing financial interests.


Introduction
Heavy metal pollution is an environmental issue that has become a global problem. The production and emission of heavy metals has increased along with increased industrial development. This has led to increasing concern over food safety due to soil polluted with anthropogenic heavy metals released from industry or agriculture, such as smelting industries, residues from metalliferous mines, pesticides, fertilizers, and municipal composts. [1][2][3][4][5][6][7][8][9][10][11][12][13][14] Heavy metals are chemical elements that have a relatively high density, strong toxic effects and pose an environmental threat. 15 Heavy metals are of considerable environmental concern due to their toxicity, many sources, non-biodegradable properties, and accumulative behaviors. 16 The presence of heavy metals in foods poses serious health hazards, depending on their relative levels. The ability of plants to accumulate metals and possibly other contaminants varies with both the nature of the plant species and the nature of the metal contaminant. Cereals, in this case Zea mays L (maize), are known to be good accumulators of contaminants. 17 Agricultural soils in many parts of the world are slightly to moderately contaminated by heavy metal toxicity, such as cadmium (Cd), copper (Cu), zinc (Zn), nickel (Ni), cobalt (Co), chromium (Cr), lead (Pb), and arsenic (As). This could be due to long-term use of phosphatic fertilizers, sewage sludge application, dust horn smelters, industrial waste and poor watering practices in agricultural lands. 18-20 The primary response of plants is the generation of reactive oxygen species upon exposure to high levels of heavy metals. Various metals either generate reactive oxygen species directly through Haber-Weiss reactions or overproduce reactive oxygen species and the Review occurrence of oxidative stress in plants could be the indirect consequence of heavy metal toxicity. 21, 22 The indirect mechanisms include their interactions with the antioxidant system, disrupting the electron transport chain or disturbing the metabolism of essential elements. 23-25 One of the most deleterious effects induced by heavy metals exposure in plants is lipid peroxidation, which can directly cause biomembrane deterioration. Malondialdehyde, one of the decomposition products of polyunsaturated fatty acids of a membrane, is regarded as a reliable indicator of oxidative stress. 26 Such toxic elements are considered soil pollutants due to their widespread occurrence, and their acute and chronic toxic effect on plants grown.
Zea mays L. is an annual cereal plant of the Gramineae family native to Mexico, it is one of the oldest and widely cultivated cereals and serves as food for humans and feed for livestock. 27,28 Zea mays L. has been a major food source for humans since ancient times. It is a domesticated plant and has many beneficial uses for people and animals. Maize is one of the most intensively cultivated cereals worldwide. It is a basic staple food grain for large parts of world and is the main food energy source in developing countries, including Africa, Latin America, and Asia. 29, 30 In Nigeria, maize can be found in every city and village where it is consumed as a staple food. 28 Zea mays L. is the third most important cereal grain worldwide, after wheat and rice. 31 All parts of the crop can be used for food and non-food products, it can also be used in animal feed as a feedstock source in agricultural complexes. 32 In industrialized countries, maize is largely used as livestock feed and as raw material for industrial production. It contains the vitamins A, B, C and E, including mineral salts and essential trace elements such as carotene, thiamine, ascorbic acid and tocopherol. 33 Zea mays L. is a widely cropped annual cereal that grows rapidly, produces extensive fibrous root systems with large shoot biomass yield per hectare, withstands adverse conditions, and produces abundant seeds with ease of cultivation under repeated cropping. To date, over 400 taxa of plant hyperaccumulators of heavy metals have been identified, but most of them are low biomass producers and exotic species. There is a need to supplement the list of plants available for phytoextraction. The potential use of maize, a robust tropical cereal crop in phytoextraction technology and possible utilization of the by-product is especially advocated for developing countries with scarce funds available for environmental restoration.
Several studies on the effects of bioaccumulation in plants through uptake of heavy metals from soils at high concentrations have been carried out and indicate great health risks, taking into consideration food chain implications. Utilization of food crops contaminated with heavy metals is a major food chain route for human exposure, especially those under continuous cultivation. The cultivation of such plants in contaminated soil represents a potential risk since the vegetal tissues can accumulate heavy metals. 34 Heavy metals become toxic when they are not metabolized by the body and accumulate in soft tissues. 35 Chronic ingestion of toxic metals has undesirable impacts on humans and the associated harmful impacts become perceptible only after several years of exposure. 36 The bioaccumulation factor (BAF) is used to quantify the bioaccumulation effect of maize in the uptake of heavy metal from soil. The BAF evaluates the effectiveness of a plant in metal accumulation and translocation. 37 Heavy metal contaminants not only represent a threat to agricultural product safety, but also harm the immune, reproductive, and nervous systems of organisms after entering their bodies through ingestion. Therefore, the transfer and accumulation of heavy metals in soil-plant systems has become an important research topic. We aimed to examine the ability of Zea mays to accumulate heavy metals and assess the bioaccumulation factor (BAF) by collecting, collating, and analysing data on heavy metal concentrations in Zea mays.

Methods
Data related to the research topics was collected from published journals, articles, textbooks and dissertations sourced from PubMed, Google Scholar, JSTOR, Science Direct and AJOL.

Review
(PRISMA) flow diagram indicating the number of articles that were identified, screened, and included in the current review is shown in Figure 1. Search terms were heavy metals, Zea mays, and bioaccumulation.

Determination of bioaccumulation factor
The BAF is the ratio of the concentration of heavy metals in plants and in soils. It is an indicator of a plant's capacity to accumulate heavy metals. 38 The BAF was calculated using Equation 1:

Equation 1:
where, P i is the concentration of a heavy metal in plants (mg/kg −1 ); and S i is the concentration of the same heavy metal in the soil where the plant grows (mg/kg −1 ). BAF was provided in the following articles shown in Table 1.
However, Equation 1 was applied in the articles presented in Table 2 where the P i (concentration of heavy metal in Zea mays) and S i (concentration of the same heavy metal in the soil) was provided.

Statistical analysis
Data retrieved were analyzed on the stated hypothesis using descriptive statistics. Descriptive statistics were used to analyze and perform a one-sample Student's t-test to test the hypothesis that the mean concentration of each heavy metal in Zea mays is not significantly different from the permissible limit set by the World Health Organization (WHO).

Results
Bioaccumulation of heavy metals, including Cd, Cr, Pb, Cu and Zn in Zea mays has been established by several studies worldwide using different indicators and parameters. Tables 3-7 show the bioaccumulation of selected heavy metals in Zea mays. Tables 8-12 show the BAF of soils across different sites and studies. The BAFs of Cd, Pb, Cr, Zn, and Cu in Zea mays from the study areas fall within the ranges of 0-0.95, 0-1.20, 0-1.89, 0.03-0.99, and 0.011-0.99, for dumpsites, industrially polluted soil, mining and smelting sites, municipal waste water irrigated soils and a battery waste dumpsite, respectively. Table 13 shows the concentration of the selected heavy metals in Zea mays from various research data.
A one-sample Student's t-test (Table 14) was performed to test the hypothesis that the mean concentration of Cd in Zea mays is not significantly different from the permissible limit set by the WHO/ Food and Agriculture Organization for Cd in food. 67 The permissible limit for Cd in all foods is set at 0.1 mg/kg.

The mean concentrations of Cd in
Zea mays (mean = 4.31) was not significantly different (p=0.097) from the WHO value of 0.1 mg/kg, test statistic (t)(17) = 1.76, p=0.09. The

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Table 14 -One Sample t-Test for Concentration of Cadmium in Maize Table 15 -One Sample t-Test for Concentration of Lead in Maize Table 16 -One Sample t-Test for Concentration of Chromium in Maize
Bioaccumulation Factor in Zea mays Review interval contains zero indicates that the test would not be rejected at the α = .05 level, and there is not significant evidence that the mean concentration of Cr is different from 1 mg/kg.
A one-sample Student's t-test (Table 17) was performed to test the hypothesis that the mean concentration of Cu in Zea mays is not significantly different from the permissible limit set by WHO for Cu in food. The permissible limit for Cu in all foods is set at 10 mg/kg.

The mean concentrations of Cu in
Zea mays (mean = 13.37, standard deviation = 11.33, number = 13) were not significantly different from the hypothesized value of 10 mg/kg, t(12) = 1.07, p=0.30. The confidence interval above is given as -3.47060, 10.21752. Thus, the fact that this interval contains zero indicates that the test would not be rejected at the α = .05 level, and there is not significant evidence that the mean concentration of Cu is different from 10 mg/kg.
Copper is an essential element in mammalian nutrition as a component of metallo-enzymes in which it acts as an electron donor or acceptor. Conversely, exposure to high levels of Cu can result in a number of adverse health effects. 70

Discussion
Maize is capable of bioaccumulating heavy metals from contaminated soils by translocating them from roots to shoots. Certain metals (e.g. Cd and Pb) have been reportedly accumulated by maize above the level used to define metal hyperaccumulation. Based on its capability of heavy metal uptake and sensitivity to high levels of metal pollution, maize is considered to be an accumulator and a metal tolerant plant, especially for Cd and Zn. 71 One of the key aspects of the acceptance of phytoextraction pertains to its performance, ultimate utilization of by products and its overall economic viability.
However, the transfer and accumulation of heavy metals from soil to plants is an extremely complex process affected by multiple factors, which exert different influences on the process by means of various mechanisms. Some of the major influencing factors include the chemical forms of the heavy metals, pH of the soil, the soil organic matter content, plant species, climatic conditions, and irrigation with polluted water. 72-77 As soils in different areas differ greatly in physical and chemical properties, the mechanisms of heavy metal transfer and accumulation in soilplant systems is complex, and may be the cause for variations in Zea mays accumulation of heavy metals in the literature. 78 There are a number of factors which influence uptake. Organic acid exudation by plants is a major factor governing the transfer and accumulation of heavy metals as they affect the uptake of heavy metals by altering the rhizosphere processes responsible for nutrient uptake. Flavonoid exudation can influence nutrient cycles by interacting with proteins and making protein nitrogen more resistant to microbial degradation and could indirectly affect soil pH, thus influencing heavy metals activity. Clay minerals and other soil colloids may also influence the bioavailability of heavy metals (a study by Zhou and Li (1996) suggested that for a given soil pH, increasing the proportion of particles with a size smaller than 0.002 mm can increase the soil capacity for Zn adsorption, thereby limiting the transfer of Zn to plants). Microbes are another factor affecting heavy metals uptake by  87 The number of microbes around the roots is higher than that in other parts of the soil. Bacteria and fungi surrounding plant roots can promote plant uptake of heavy metals by changing heavy metals activity. 88 For example, some bacteria can reduce As, mercury, and selenium, while others can oxidize iron and As. 89 Among the various mechanisms of plant absorption, passive uptake via micro pores in the cell walls of root cells is the main method by which heavy metals access plants; chemical species with a high redox activity and chelating agents in soil may affect heavy metal uptake and accumulation in plants by changing their chemical form and thus their availability for plants. 90 Nitrogen in soil represents another important factor influencing the transfer of heavy metals in soil-plant systems. It affects the bioavailability of heavy metals mainly by altering soil acidity. 91-94 Soil pH is another factor influencing uptake of heavy metals from the soil. Among heavy metals, Cd is the most sensitive to soil pH. 95, 96 In addition, ammonium ions can displace trace metals in exchangeable forms or facilitate their release from soil colloids. 97 The changes in concentration of soil-free bases and pH resulting from the dissolution and diffusion of ammonia nitrogen in soil in turn may change the solubility of heavy metals in soil. 98 The mobility of heavy metals in soilplant systems is also affected by the way heavy metals enter the plants.
Chemical elements are primarily uptaken by roots from the soil or by leaves from the atmosphere. Apart from differences among various plant species and cultivars, the overall combination of soil physical and chemical properties controls both the rate and extent of metal uptake. 99  Other plant parts such as stem, stalk and silk were also found to contain these metals, indicating that they are unsafe for use as animal feedstock.
The current study revealed that dumpsites are sinks for elevated levels of heavy metals. It is important to note that if peasant farmers continue to cultivate maize and other arable crops on abandoned dumpsites, this will increase the levels of heavy metals which may eventually enter the food chain and present possible adverse human health effects. Heavy metal accumulation in soils and plants is of increasing concern due to the potential human health risks. Heavy metal contaminants not only represent a threat to agricultural product safety, but also harm to immune, reproductive, and nervous systems of organisms after entering their bodies through ingestion. This eventually leads to food chain contamination, which is an important pathway for entry of toxic pollutants into the human body. Heavy metals uptake by plants and successive accumulation in human tissues and biomagnifications through the food chain causes both human health and environment concerns. Since the toxic heavy metal concentrations in the most commonly consumed parts of the maize plant are high, there is a tendency for these metals to transfer to both animals (through leaves and stem used as fodder) and humans, presenting human health risks. Thus, as maize plants grown on the topsoil of waste dumpsites have shown active phytoextraction via the root as well as high bioaccumulative properties, this study recommends that the maize grown near dumpsites is unfit for human and animal consumption.
These crops could expose residents and livestock to the undesired effects of heavy metal toxicity.

Conclusions
An analysis of the available data on Zea mays revealed that the concentrations of Cd, Cr, Pb, Cu, and Zn are high in Zea mays. Metals uptake by plants from soil reduces crop productivity by inhibiting physiological metabolism. Accumulation of heavy metals in plants and biomagnification presents a threat to human and environmental health. Excessive accumulation of heavy metals in agricultural soils often leads to elevated heavy metal uptake by crops, and thus affects food quality and safety. 120 Food chain contamination is an important pathway for the entry of toxic pollutants into the human body. Heavy metals have been proven to be toxic to both humans and the environment. Therefore, regular environmental monitoring and restoration is imperative to determine that soils used for maize farming are not contaminated with heavy metals.
Owing to their toxicity and possible bioaccumulation, these compounds should be subject to mandatory monitoring. Governments should promote harmonized data collection, research, legislation and regulations, and consider the use of indicators. Assessments determining the chemical concentration scenario and the use of biomarkers should provide useful data to set standards and guideline values designed to protect human and environmental health from heavy metal contaminants. Exposure measurements are essential for the protection of high-risk populations and subgroups. Furthermore, governments should, when setting acceptable levels or criteria related to chemicals, take into consideration the potential enhanced exposures and/or vulnerabilities of children.
The ability of Zea mays to accumulate heavy metals from soil is significantly affected by a number of factors aside from the concentration of heavy metals in soil. However, based on the outcomes of the present study, it was concluded that Zea mays is capable of accumulating all selected heavy metals from soil over a wide range of environmental conditions.